Transcranial alternating current stimulation entrains alpha oscillations by preferential phase synchronization of fast-spiking cortical neurons to stimulation waveform

AbstractComputational modeling and human studies suggest that transcranial alternating current stimulation (tACS) modulates alpha oscillations by entrainment. Yet, a direct examination of how tACS interacts with neuronal spiking activity that gives rise to the alpha oscillation in the thalamo-cortical system has been lacking. Here, we demonstrate how tACS entrains endogenous alpha oscillations in head-fixed awake ferrets. We first show that endogenous alpha oscillations in the posterior parietal cortex drive the primary visual cortex and the higher-order visual thalamus. Spike-field coherence is largest for the alpha frequency band, and presumed fast-spiking inhibitory interneurons exhibit strongest coupling to this oscillation. We then apply alpha-tACS that results in a field strength comparable to what is commonly used in humans (<0.5 mV/mm). Both in these ferret experiments and in a computational model of the thalamo-cortical system, tACS entrains alpha oscillations by following the theoretically predicted Arnold tongue. Intriguingly, the fast-spiking inhibitory interneurons exhibit a stronger entrainment response to tACS in both the ferret experiments and the computational model, likely due to their stronger endogenous coupling to the alpha oscillation. Our findings demonstrate the in vivo mechanism of action for the modulation of the alpha oscillation by tACS.

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Transcranial Alternating Current Stimulation (tACS) Entrains Alpha Oscillations by Preferential Phase Synchronization of Fast-Spiking Cortical Neurons to Stimulation Waveform

10.1101/563163 ◽

2019 ◽

Cited By ~ 3

Author(s):

Ehsan Negahbani ◽

Iain M. Stitt ◽

Marshall Davey ◽

Thien T. Doan ◽

Moritz Dannhauer ◽

...

Keyword(s):

Electric Field ◽

Electric Fields ◽

Cortical Neurons ◽

Posterior Parietal Cortex ◽

Phase Synchronization ◽

Alternating Current ◽

Arnold Tongue ◽

Transcranial Alternating Current Stimulation ◽

Neuronal Oscillators

SummaryModeling studies predict that transcranial alternating current stimulation (tACS) entrains brain oscillations, yet direct examination has been lacking or potentially contaminated by stimulation artefact. Here we first demonstrate how the posterior parietal cortex drives primary visual cortex and thalamic LP in the alpha-band in head-fixed awake ferrets. The spike-field synchrony is maximum within alpha frequency, and more prominent for narrow-spiking neurons than broad-spiking ones. Guided by a validated model of electric field distribution, we produced electric fields comparable to those in humans and primates (< 0.5 mV/mm). We found evidence to support the model-driven predictions of how tACS entrains neural oscillations as explained by the triangular Arnold tongue pattern. In agreement with the stronger spike-field coupling of narrow-spiking cells, tACS more strongly entrained this cell population. Our findings provide the firstin vivoevidence of how tACS with electric field amplitudes used in human studies entrains neuronal oscillators.

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Examining motor evoked potential amplitude and short‐interval intracortical inhibition on the up‐going and down‐going phases of a transcranial alternating current stimulation (tacs) imposed alpha oscillation

European Journal of Neuroscience ◽

10.1111/ejn.15124 ◽

2021 ◽

Author(s):

Ann‐Maree Vallence ◽

Kathryn Dansie ◽

Mitchell R. Goldsworthy ◽

Suzanne M. McAllister ◽

Ruiting Yang ◽

...

Keyword(s):

Evoked Potential ◽

Short Interval ◽

Motor Evoked Potential ◽

Intracortical Inhibition ◽

Alternating Current ◽

Potential Amplitude ◽

Alpha Oscillation ◽

Transcranial Alternating Current Stimulation

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Transient amplitude modulation of alpha-band oscillations by short-time intermittent closed-loop tACS

10.1101/2020.01.23.916676 ◽

2020 ◽

Author(s):

G. Zarubin ◽

C. Gundlach ◽

V. Nikulin ◽

A. Villringer ◽

M. Bogdan

Keyword(s):

Individual Differences ◽

Visual System ◽

Amplitude Modulation ◽

Closed Loop ◽

Alternating Current ◽

Stimulation Protocol ◽

Spatial Filters ◽

Alpha Oscillations ◽

Transcranial Alternating Current Stimulation ◽

Short Time

AbstractNon-invasive brain stimulation techniques such as transcranial alternating current stimulation (tACS) have recently become extensively utilized due to their potential to modulate ongoing neuronal oscillatory activity and consequently to induce cortical plasticity relevant for various cognitive functions. However, the neurophysiological basis for stimulation effects as well as their inter-individual differences are not yet understood. In the present study we used a closed-loop EEG transcranial alternating current stimulation protocol (EEG-tACS) to examine the modulation of alpha oscillations generated in occipito-parietal areas. In particular, we investigated the effects of a repeated short-time intermittent stimulation protocol (1 s in every trial) applied over the visual cortex (Cz and Oz) and adjusted according to the phase and frequency of visual alpha oscillations on the amplitude of these oscillations. Based on previous findings, we expected higher increases in alpha amplitudes for tACS applied in-phase with ongoing oscillations as compared to an application in anti-phase and this modulation to be present in low-alpha amplitude states of the visual system (eyes opened) but not high (eyes closed).Contrary to our expectations, we found a transient suppression of alpha power in inter-individually derived spatially specific parieto-occipital components obtained via the estimation of spatial filters by using the common spatial patterns approach. The amplitude modulation was independent of the phase relationship between tACS signal and alpha oscillations, and the state of the visual system manipulated via closed- and open-eye conditions. It was also absent in conventionally analyzed single-channel and multi-channel data from an average parieto-occipital region.The fact that the tACS modulation of oscillations was phase-independent suggests that mechanisms driving the effects of tACS may not be explained by entrainment alone, but rather require neuroplastic changes or transient disruption of neural oscillations. Our study also supports the notion that the response to tACS is subject specific, where the modulatory effects are shaped by the interplay between the stimulation and different alpha generators. This favors stimulation protocols as well as analysis regimes exploiting inter-individual differences, such as spatial filters to reveal otherwise hidden stimulation effects and, thereby, comprehensively induce and study the effects and underlying mechanisms of tACS.

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A computational model to guide the functional decoupling of two brain regions with transcranial alternating current stimulation

Brain Stimulation ◽

10.1016/j.brs.2021.10.082 ◽

2021 ◽

Vol 14 (6) ◽

pp. 1613

Author(s):

Jesús Cabrera-Álvarez ◽

Gianluca Susi ◽

Jaime Sánchez-Claro ◽

Martín Carrasco ◽

Alberto del Cerro ◽

...

Keyword(s):

Computational Model ◽

Alternating Current ◽

Brain Regions ◽

Transcranial Alternating Current Stimulation

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Transcranial alternating current stimulation (tACS): from basic mechanisms towards first applications in psychiatry

European Archives of Psychiatry and Clinical Neuroscience ◽

10.1007/s00406-020-01209-9 ◽

2020 ◽

Cited By ~ 1

Author(s):

Osama Elyamany ◽

Gregor Leicht ◽

Christoph S. Herrmann ◽

Christoph Mulert

Keyword(s):

Psychiatric Disorders ◽

Cortical Neurons ◽

Alternating Current ◽

Brain Network ◽

Brain Oscillations ◽

Serious Adverse Events ◽

Double Blind ◽

Response Predictors ◽

Transcranial Alternating Current Stimulation ◽

The Brain

AbstractTranscranial alternating current stimulation (tACS) is a unique form of non-invasive brain stimulation. Sinusoidal alternating electric currents are delivered to the scalp to affect mostly cortical neurons. tACS is supposed to modulate brain function and, in turn, cognitive processes by entraining brain oscillations and inducing long-term synaptic plasticity. Therefore, tACS has been investigated in cognitive neuroscience, but only recently, it has been also introduced in psychiatric clinical trials. This review describes current concepts and first findings of applying tACS as a potential therapeutic tool in the field of psychiatry. The current understanding of its mechanisms of action is explained, bridging cellular neuronal activity and the brain network mechanism. Revisiting the relevance of altered brain oscillations found in six major psychiatric disorders, putative targets for the management of mental disorders using tACS are discussed. A systematic literature search on PubMed was conducted to report findings of the clinical studies applying tACS in patients with psychiatric conditions. In conclusion, the initial results may support the feasibility of tACS in clinical psychiatric populations without serious adverse events. Moreover, these results showed the ability of tACS to reset disturbed brain oscillations, and thus to improve behavioural outcomes. In addition to its potential therapeutic role, the reactivity of the brain circuits to tACS could serve as a possible tool to determine the diagnosis, classification or prognosis of psychiatric disorders. Future double-blind randomised controlled trials are necessary to answer currently unresolved questions. They may aim to detect response predictors and control for various confounding factors.

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Bilateral Gamma/Delta Transcranial Alternating Current Stimulation Affects Interhemispheric Speech Sound Integration

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01498 ◽

2020 ◽

Vol 32 (7) ◽

pp. 1242-1250 ◽

Cited By ~ 1

Author(s):

Basil C. Preisig ◽

Matthias J. Sjerps ◽

Alexis Hervais-Adelman ◽

Anne Kösem ◽

Peter Hagoort ◽

...

Keyword(s):

Auditory Cortex ◽

Phase Synchronization ◽

Speech Sound ◽

Alternating Current ◽

Phase Lag ◽

Disruptive Effect ◽

Phase Coupling ◽

Gamma Frequency ◽

Transcranial Alternating Current Stimulation ◽

Speech Cues

Perceiving speech requires the integration of different speech cues, that is, formants. When the speech signal is split so that different cues are presented to the right and left ear (dichotic listening), comprehension requires the integration of binaural information. Based on prior electrophysiological evidence, we hypothesized that the integration of dichotically presented speech cues is enabled by interhemispheric phase synchronization between primary and secondary auditory cortex in the gamma frequency band. We tested this hypothesis by applying transcranial alternating current stimulation (TACS) bilaterally above the superior temporal lobe to induce or disrupt interhemispheric gamma-phase coupling. In contrast to initial predictions, we found that gamma TACS applied in-phase above the two hemispheres (interhemispheric lag 0°) perturbs interhemispheric integration of speech cues, possibly because the applied stimulation perturbs an inherent phase lag between the left and right auditory cortex. We also observed this disruptive effect when applying antiphasic delta TACS (interhemispheric lag 180°). We conclude that interhemispheric phase coupling plays a functional role in interhemispheric speech integration. The direction of this effect may depend on the stimulation frequency.

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Reduction in left frontal alpha oscillations by transcranial alternating current stimulation in major depressive disorder is context-dependent in a randomized clinical trial

Biological Psychiatry Cognitive Neuroscience and Neuroimaging ◽

10.1016/j.bpsc.2021.07.001 ◽

2021 ◽

Author(s):

Justin Riddle ◽

Morgan L. Alexander ◽

Crystal Edler Schiller ◽

David R. Rubinow ◽

Flavio Frohlich

Keyword(s):

Clinical Trial ◽

Major Depressive Disorder ◽

Depressive Disorder ◽

Randomized Clinical Trial ◽

Alternating Current ◽

Major Depressive ◽

Alpha Oscillations ◽

Transcranial Alternating Current Stimulation ◽

Context Dependent

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Reduction in left frontal alpha oscillations by transcranial alternating current stimulation in major depressive disorder is context-dependent in a randomized-clinical trial

10.1101/2021.06.17.21258764 ◽

2021 ◽

Author(s):

Justin Riddle ◽

Morgan L. Alexander ◽

Crystal Edler Schiller ◽

David R. Rubinow ◽

Flavio Frohlich

Keyword(s):

Clinical Trial ◽

Major Depressive Disorder ◽

Depressive Disorder ◽

Alpha Power ◽

Single Session ◽

Major Depressive ◽

Alpha Oscillations ◽

Alpha Frequency ◽

Alpha Oscillation ◽

Transcranial Alternating Current Stimulation

Background: Left frontal alpha oscillations are associated with decreased approach motivation and have been proposed as a target for non-invasive brain stimulation for the treatment of depression and anhedonia. Indeed, transcranial alternating current stimulation (tACS) at the alpha frequency reduced left frontal alpha power and was associated with a higher response rate than placebo stimulation in patients with major depressive disorder (MDD) in a recent double-blind placebo controlled clinical trial. Methods: In this current study, we aimed to replicate such successful target engagement by delineating the effects of a single session of bifrontal tACS at the individualized alpha frequency (IAF-tACS) on alpha oscillations in patients with MDD. Electrical brain activity was recorded during rest and while viewing emotionally-salient images before and after stimulation to investigate if the modulation of alpha oscillation by tACS exhibited specificity with regards to valence. Results: In agreement with the previous study of tACS in MDD, we found that a single session of bifrontal IAF-tACS reduced left frontal alpha power during the resting state when compared to placebo. Furthermore, the reduction of left frontal alpha oscillation by tACS was specific for stimuli with positive valence. In contrast, these effects on left frontal alpha power were not found in healthy control participants. Conclusion: Together these results support an important role of tACS in reducing left frontal alpha oscillations as a future treatment for MDD. National Clinical Trial: NCT03449979, Single Session of tACS in a Depressive Episode (SSDE) https://www.clinicaltrials.gov/ct2/show/NCT03449979 .

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